Pasquier, J. | Search bioRxiv

bioRxiv2017

Evolution of gene expression after whole-genome duplication: new insights from the spotted gar genome

Whole genome duplications (WGD) are important evolutionary events. Our understanding of underlying mechanisms, including the evolution of duplicated genes after WGD, however remains incomplete. Teleost fish experienced a common WGD (teleost-specific genome duplication, or TGD) followed by a dramatic adaptive radiation leading to more than half of all vertebrate species. The analysis of gene expression patterns following TGD at the genome level has been limited by the lack of suitable genomic resources. The recent concomitant release of the genome sequence of spotted gar (a representative of holosteans, the closest lineage of teleosts that lacks the TGD) and the tissue-specific gene expression repertoires of over 20 holostean and teleostean fish species, including spotted gar, zebrafish and medaka (the PhyloFish project), offered a unique opportunity to study the evolution of gene expression following TGD in teleosts. We show that most TGD duplicates gained their current status (loss of one duplicate gene or retention of both duplicates) relatively rapidly after TGD (i.e. prior to the divergence of medaka and zebrafish lineages). The loss of one duplicate is the most common fate after TGD with a probability of approximately 80%. In addition, the fate of duplicate genes after TGD, including subfunctionalization, neofunctionalization, or retention of two similar copies occurred not only before, but also after the radiation of species tested, in consistency with a role of the TGD in speciation and/or evolution of gene function. Finally, we report novel cases of TGD ohnolog subfunctionalization and neofunctionalization that further illustrate the importance of these processes.

evolutionary biology↗

bioRxiv2017

Double Maternal Effect: Duplicated Nucleoplasmin 2 Genes, npm2a And npm2b, Are Shared By Fish And Tetrapods, And Have Distinct And Essential Roles In Early Embryogenesis

Nucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic events through its function as a histone chaperone that remodels chromatin. Here we report the existence of two npm2 (npm2a and npm2b) genes in zebrafish. We examined the evolution of npm2a and npm2b in a variety of vertebrates, their potential phylogenetic relationships, and their biological functions using knockout models via the CRISPR/cas9 system. We demonstrated that the two npm2 duplicates exist in a wide range of vertebrates, including sharks, ray-finned fish, amphibians, and sauropsids, while npm2a was lost in Coelacanth and mammals, as well as some specific teleost lineages. Using phylogeny and synteny analyses, we traced their origins to the early stages of vertebrate evolution. Our findings suggested that npm2a and npm2b resulted from an ancient local gene duplication, and their functions diverged although key protein domains were conserved. We then investigated their functions by examining their tissue distribution in a wide variety of species and found that they shared ovarian-specific expression, a key feature of maternal-effect genes. We also showed that both npm2a and npm2b are maternally-inherited transcripts in vertebrates. Moreover, we used zebrafish knockouts to demonstrate that npm2a and npm2b play essential, but distinct, roles in early embryogenesis. npm2a functions very early during embryogenesis, at or immediately after fertilization, while npm2b is involved in processes leading up to or during zygotic genome activation. These novel findings will broaden our knowledge on the evolutionary diversity of maternal-effect genes and underlying mechanisms that contribute to vertebrate reproductive success.\n\nAuthor SummaryThe protein and transcript of the npm2 gene have been previously demonstrated as maternal contributions to embryos of several vertebrates. Recently, two npm2 genes, denoted here as npm2a and npm2b, were discovered in zebrafish. This study was conducted to explore the evolutionary origin and changes that occurred that culminated in their current functions. We found that an ancient local duplication of the ancestral npm2 gene created the current two forms, and while most vertebrates retained both genes, notably, mammals and certain species of fish lost npm2a and, albeit rarely, both npm2a and npm2b. Our functional analyses showed that npm2a and npm2b have diverse but essential functions during embryogenesis, as npm2a mutants failed to undergo development at the earliest stage while npm2b mutants developed, although abnormally, until the zygotic genome activation stage after which their development was arrested followed subsequently by death. Our study is the first to clearly demonstrate the evolution, diversification, and functional analyses of the npm2 genes, which are essential maternal factors that are required for proper embryonic development and survival.

evolutionary biology↗